Lasting alteration of spatial orientation induced by passive motion in rabbits and its possible relevance to mal de débarquement syndrome

Abstract

BackgroundMal de débarquement syndrome (MdDS) is a chronic disorder of spatial orientation with a persistent false sensation of self-motion, whose onset typically follows prolonged exposure to passive motion of a transport vehicle. Development of similar but transient after-sensations mimicking the exposed motion and associated postural instability, indicative of central vestibular adaptation, are common. The cause of MdDS is thought to be a subsequent failure to readapt to a stationary environment. However, vestibular plasticity pertinent to this illness has not been studied sufficiently. Because the rabbit's eye movement is sensitive to three-dimensional spatial orientation, characterizing maladaptation of the vestibulo-ocular reflex (VOR) induced in the animal may open an approach to understanding MdDS.MethodsThree rabbits underwent a series of 2-h conditioning with an unnatural repetitive motion that involved a complex combination of roll, pitch, and yaw movements in a head-based reference frame, consisting of periodic rolling in darkness in a frame of reference that rotated about an earth-vertical axis. Eye movement in three dimensions was sampled during the conditioning stimulus as well as during test stimuli before and up to several days after conditioning.ResultsDuring roll-while-rotating conditioning, the roll component of the VOR was compensatory to the oscillation about the corresponding axis, but the pitch component was not, initially prominently phase-leading the head pitch motion but subsequently becoming patently phase-delayed. Unidirectional yaw nystagmus, weak but directionally compensatory to the earth-vertical axis rotation, was seen throughout the period of conditioning. After conditioning, simple side-to-side rolling induced an abnormal yaw ocular drift in the direction that opposed the nystagmus seen during conditioning, indicating a maladaptive change in spatial orientation. The impact of conditioning appeared to be partially retained even after 1 week and could be partially reversed or cumulated depending on the rotation direction in the subsequent conditioning.ConclusionThe observed reversible long-term maladaptation of spatial orientation as well as the depth of knowledge available in relation to the vestibular cerebellar circuits in this species support the potential utility of a rabbit model in MdDS research.

Guideline for standardized approach in the treatment of the Mal de Debarquement syndrome

“…The results revealed that, following conditioning, an unusual ocular drift occurred in the yaw plane during rolling maneuvres, moving in the opposite direction to the nystagmus observed during conditioning. This finding suggests a maladaptive alteration and emphasizes the value of this rabbit model in MdDS research (12).…”

“…Nineteen patients came back for a second treatment session, six for a third, and five for a fourth. From the 101 individual patients, 81 are female of on average (SD) 45 (15) years old and between 18 and 79 years of age, and 20 male of on average (SD) 39 (12) years old and between 24 and 61 years of age. Patients had had complaints for a median (median absolute deviation (MAD)) of 3.7 (1.78) years and between 1 month and 21 years, before they received the OKS treatment.…”

“…In a more recent study, three rabbits were exposed to an unnatural repetitive motion for 2 h that involved intricate combinations of roll, pitch, and yaw movements in a head-based reference frame ( 12 ). The head-based frame was used to describe the six degrees of freedom, translation and rotation around the x, y, and z-axis with the rabbit’s head as reference.…”

Symptom reduction in mal de débarquement syndrome with attenuation of the velocity storage contribution in the central vestibular pathways

“…Further support for the velocity storage involvement in MdDS comes from a sham-controlled study, which demonstrated a treatment effect when head tilts were coupled with large-field visual motion as in the original protocol but not with a non-moving but otherwise identical visual pattern (45). A recent sequel animal-based study also supports that the effect of VOR maladaptation can be systematically cumulated or reversed by the choice of the vestibular stimulus (46). Together, VOR readaptation has come to be recognized as the first effective treatment for MdDS (47).…”